Wakefulness enables animals to interface adaptively with the environment. Paradoxically, in insects to humans, the efficacy of wakefulness depends on daily sleep, a mysterious, usually quiescent state of reduced environmental awareness. However, several birds fly non-stop for days, weeks or months without landing, questioning whether and how they sleep. It is commonly assumed that such birds sleep with one cerebral hemisphere at a time (i.e. unihemispherically) and with only the corresponding eye closed, as observed in swimming dolphins. However, the discovery that birds on land can perform adaptively despite sleeping very little raised the possibility that birds forgo sleep during long flights. In the first study to measure the brain state of birds during long flights, great frigatebirds (Fregata minor) slept, but only during soaring and gliding flight. Although sleep was more unihemispheric in flight than on land, sleep also occurred with both brain hemispheres, indicating that having at least one hemisphere awake is not required to maintain the aerodynamic control of flight. Nonetheless, soaring frigatebirds appeared to use unihemispheric sleep to watch where they were going while circling in rising air currents. Despite being able to engage in all types of sleep in flight, the birds only slept for 0.7 h d⁻¹ during flights lasting up to 10 days. By contrast, once back on land they slept 12.8 h d⁻¹. This suggests that the ecological demands for attention usually exceeded that afforded by sleeping unihemispherically. The ability to interface adaptively with the environment despite sleeping very little challenges commonly held views regarding sleep, and therefore serves as a powerful system for examining the functions of sleep and the consequences of its loss. © 2016 The Author(s) Published by the Royal Society. All rights reserved.